The Tomato Brown Rugose Fruit Virus Movement Protein Overcomes Tm-22 Resistance in Tomato While Attenuating Viral Transport
Tomato brown rugose fruit virus is a new virus species in the Tobamovirus genus, causing substantial damage to tomato crops. Reports of recent tomato brown rugose fruit virus (ToBRFV) outbreaks from around the world indicate an emerging global epidemic. ToBRFV overcomes all tobamovirus resistances i...
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| Format: | Article |
| Language: | English |
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The American Phytopathological Society
2021-09-01
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| Series: | Molecular Plant-Microbe Interactions |
| Subjects: | |
| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-01-21-0023-R |
| _version_ | 1819045883479588864 |
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| author | Hagit Hak Ziv Spiegelman |
| author_facet | Hagit Hak Ziv Spiegelman |
| author_sort | Hagit Hak |
| collection | DOAJ |
| description | Tomato brown rugose fruit virus is a new virus species in the Tobamovirus genus, causing substantial damage to tomato crops. Reports of recent tomato brown rugose fruit virus (ToBRFV) outbreaks from around the world indicate an emerging global epidemic. ToBRFV overcomes all tobamovirus resistances in tomato, including the durable Tm-22 resistance gene, which had been effective against multiple tobamoviruses. Here, we show that the ToBRFV movement protein (MPToBRFV) enables the virus to evade Tm-22 resistance. Transient expression of MPToBRFV failed to activate the Tm-22 resistance response. Replacement of the original MP sequence of tomato mosaic virus (ToMV) with MPToBRFV enabled this recombinant virus to infect Tm-22-resistant plants. Using hybrid protein analysis, we show that the elements required to evade Tm-22 are located between MPToBRFV amino acids 1 and 216 and not the C terminus, as previously assumed. Analysis of ToBRFV systemic infection in tomato revealed that ToBRFV spreads more slowly compared with ToMV. Interestingly, replacement of tobacco mosaic virus (TMV) and ToMV MPs with MPToBRFV caused an attenuation of systemic infection of both viruses. Cell-to-cell movement analysis showed that MPToBRFV moves less effectively compared with the TMV MP (MPTMV). These findings suggest that overcoming Tm-22 is associated with attenuated MP function. This may explain the high durability of Tm-22 resistance, which had remained unbroken for over 60 years.[Graphic: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license. |
| first_indexed | 2024-12-21T10:35:39Z |
| format | Article |
| id | doaj.art-095e2b9201504196afe481fd2c0b1753 |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-12-21T10:35:39Z |
| publishDate | 2021-09-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-095e2b9201504196afe481fd2c0b17532022-12-21T19:07:04ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062021-09-013491024103210.1094/MPMI-01-21-0023-RThe Tomato Brown Rugose Fruit Virus Movement Protein Overcomes Tm-22 Resistance in Tomato While Attenuating Viral TransportHagit Hak0Ziv Spiegelman1Department of Plant Pathology and Weed Research, Agricultural Research Organization-The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelDepartment of Plant Pathology and Weed Research, Agricultural Research Organization-The Volcani Center, 68 HaMaccabim Road, P.O.B 15159, Rishon LeZion 7505101, IsraelTomato brown rugose fruit virus is a new virus species in the Tobamovirus genus, causing substantial damage to tomato crops. Reports of recent tomato brown rugose fruit virus (ToBRFV) outbreaks from around the world indicate an emerging global epidemic. ToBRFV overcomes all tobamovirus resistances in tomato, including the durable Tm-22 resistance gene, which had been effective against multiple tobamoviruses. Here, we show that the ToBRFV movement protein (MPToBRFV) enables the virus to evade Tm-22 resistance. Transient expression of MPToBRFV failed to activate the Tm-22 resistance response. Replacement of the original MP sequence of tomato mosaic virus (ToMV) with MPToBRFV enabled this recombinant virus to infect Tm-22-resistant plants. Using hybrid protein analysis, we show that the elements required to evade Tm-22 are located between MPToBRFV amino acids 1 and 216 and not the C terminus, as previously assumed. Analysis of ToBRFV systemic infection in tomato revealed that ToBRFV spreads more slowly compared with ToMV. Interestingly, replacement of tobacco mosaic virus (TMV) and ToMV MPs with MPToBRFV caused an attenuation of systemic infection of both viruses. Cell-to-cell movement analysis showed that MPToBRFV moves less effectively compared with the TMV MP (MPTMV). These findings suggest that overcoming Tm-22 is associated with attenuated MP function. This may explain the high durability of Tm-22 resistance, which had remained unbroken for over 60 years.[Graphic: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-01-21-0023-Rmovement proteinplant immunityresistance geneSolanum lycopersicumTm-22tobamovirus |
| spellingShingle | Hagit Hak Ziv Spiegelman The Tomato Brown Rugose Fruit Virus Movement Protein Overcomes Tm-22 Resistance in Tomato While Attenuating Viral Transport Molecular Plant-Microbe Interactions movement protein plant immunity resistance gene Solanum lycopersicum Tm-22 tobamovirus |
| title | The Tomato Brown Rugose Fruit Virus Movement Protein Overcomes Tm-22 Resistance in Tomato While Attenuating Viral Transport |
| title_full | The Tomato Brown Rugose Fruit Virus Movement Protein Overcomes Tm-22 Resistance in Tomato While Attenuating Viral Transport |
| title_fullStr | The Tomato Brown Rugose Fruit Virus Movement Protein Overcomes Tm-22 Resistance in Tomato While Attenuating Viral Transport |
| title_full_unstemmed | The Tomato Brown Rugose Fruit Virus Movement Protein Overcomes Tm-22 Resistance in Tomato While Attenuating Viral Transport |
| title_short | The Tomato Brown Rugose Fruit Virus Movement Protein Overcomes Tm-22 Resistance in Tomato While Attenuating Viral Transport |
| title_sort | tomato brown rugose fruit virus movement protein overcomes tm 22 resistance in tomato while attenuating viral transport |
| topic | movement protein plant immunity resistance gene Solanum lycopersicum Tm-22 tobamovirus |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-01-21-0023-R |
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